Endophytic Beauveria bassiana of Tomato Resisted the Damage from Whitefly Bemisia tabaci by Mediating the Accumulation of Plant-Specialized Metabolites

Abstract

Beauveria bassiana acts as an endophytic fungus that controls herbivorous pests by stimulating plant defenses and inducing systemic resistance. Through multiomics analysis, 325 differential metabolites and 1739 differential expressed genes were observed in tomatoes treated with B. bassiana by root irrigation; meanwhile, 152 differential metabolites and 1002 differential genes were observed in tomatoes treated by local leaf spraying. Among the upregulated metabolites were α-solanine, 5-O-caffeoylshikimic acid, clerodendrin A, and peucedanin, which demonstrated anti-insect activity. These differential metabolites were primarily associated with alkaloid biosynthesis, flavonoid biosynthesis, and tryptophan metabolism pathways. Furthermore, the gene silencing of UDP-glucose:sterol glucosyltransferase, a gene involved in α-solanine synthesis, indicated that B. bassiana could inhibit the reproduction of whiteflies by regulating α-solanine. This study highlighted the ability of B. bassiana to modulate plant secondary metabolites and emphasized the significance of understanding and harnessing multitrophic interactions of endophytic B. bassiana for sustainable agriculture.

Keywords: Beauveria bassiana; Bemisia tabaci; metabolomic; plant secondary metabolites; tomato; transcriptomic.

Figure 1

Effects of endophytic B. bassiana on the performance of whiteflies: (A) survival rate of adult females at 3 days, (B) fecundity of adult females at 3 days, (C) survival rate of adult females at 5 days, and (D) fecundity of adult females at 5 days. The data are presented as the mean ± standard error (SE) of eight biological replicates. The error bars indicate the standard error. Different letters indicate significant differences among treatments, as determined by one-way ANOVA (p < 0.05).

Figure 2

Analysis of differential metabolites between tomatoes treated with B. bassiana and the control group: (A) clustering heatmap of quantified differential metabolites, (B) Venn diagram illustrating the differential metabolites, (C) PCA showcasing global metabolite changes in tomato leaves, (D) pathway enrichment analysis of the differential metabolites between tomatoes treated with B. bassiana by leaf spraying (BbL) and the control plants, and (E) pathway enrichment analysis of the differential metabolites between tomatoes treated with B. bassiana by root irrigation (BbR) and the control plants.

Figure 3

Overall transcriptomic changes in tomato leaves: (A) PCA of DEGs at different samples, Venn diagram depicting the comparison of (B) upregulated DEGs and (C) downregulated DEGs, (D) pathway enrichment analysis of DEGs between tomatoes treated with B. bassiana by local leaf spraying (BbL) and the control plants, and (E) pathway enrichment analysis of DEGs between tomatoes treated with B. bassiana by root irrigation (BbR) and the control plants.

Figure 4

Changes in the biosynthesis of various alkaloid metabolites and genes in B. bassiana colonization of tomato leaves compared to the control group. GAME7, cholesterol 22-hydroxylase; GAME11, 22,26-dihydroxycholesterol 16α-hydroxylase; GAME6 and GAME4, glycoalkaloid metabolism genes; and SGT1 and SGT3, UDP-glucose:sterol glucosyltransferase.

Figure 5

Changes in flavonoid metabolites and the expression of flavonoid biosynthesis genes were investigated in tomato leaves colonized by B. bassiana and in control leaves. PAL, phenylalanine ammonia lyase; 4CL, 4-coumarate-CoA ligase; CYP73A, trans-cinnamate 4-monooxygenase; HCT, shikimate O-hydroxycinnamoyltransferase; CYP98A, 5-O-(4-coumaroyl)-d-quinate 3′-monooxygenase; CHS, chalcone synthase; F3H, naringenin 3-dioxygenase; CYP75A, flavonoid 3′,5′-hydroxylase; DFR, bifunctional dihydroflavonol 4-reductase/flavanone 4-reductase; FLS, flavonol synthase; and CYP75B1, flavonoid 3′-monooxygenase.

Figure 6

Differences in the metabolites involved in the tryptophan pathway were observed between tomato leaves colonized by B. bassiana and control leaves.

Figure 7

Silencing of α-solanine synthesis genes SlSGT2 and SlSGT3: (A) quantitative analysis conducted on the gene responses for α-solanine biosynthesis, namely, SlSGT1, SlSGT2, SlSGT3, and SlSGT4, (B) silencing effect of the target gene, (C) detection of target gene silencing efficiency, (D) silencing of target genes inhibiting the production of α-solanine in tomato leaves, (E) silencing of the target gene increasing the fecundity of B. tabaci on tomato leaves within 3 days, and (F) silencing of the target gene increasing the number of nymphs on tomato leaves. All values are the mean ± standard deviation (SD), and asterisks indicate a significant difference compared to the control group using Student’s t test. (∗, p < 0.05; ∗∗, p < 0.01; and ∗∗∗, p < 0.001).